Capitalizing on diversity: An integrative approach towards the multiplicity of cellular mechanisms underlying myogenic responsiveness

Cardiovascular Research

Volumn 97, Issue 3, 2013, Pages 404-412

  Lidington, Darcy ^a,b   Schubert, Rudolf ^c   Bolz, Steffen Sebastian ^a,b,d  

^a UNIVERSITY OF TORONTO   (Canada)

^b ST MICHAEL'S HOSPITAL   (Canada)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

Calcium sensitization; Calcium signalling; Heart failure; Sphingosine 1 phosphate; Vascular smooth muscle

Indexed keywords

4 (2,6 DICHLORO 4 PYRIDINYL) 1 (1,3 DIMETHYL 4 ISOPROPYL 1H PYRAZOLO[3,4 B]PYRIDIN 6 YL)SEMICARBAZIDE; ANGIOTENSIN 1 RECEPTOR; ARACHIDONIC ACID; CALCIUM ION; CHOLINERGIC RECEPTOR; DIACYLGLYCEROL; DOPAMINE 5 RECEPTOR; ENDOTHELIN A RECEPTOR; FORMYLPEPTIDE RECEPTOR LIKE 1; G PROTEIN COUPLED RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN; HISTAMINE H1 RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MYOSIN LIGHT CHAIN; MYOSIN LIGHT CHAIN 20; PARATHYROID HORMONE RECEPTOR 1; PHENYLEPHRINE; PHOSPHOLIPASE A2; PHOSPHOLIPASE C; PROTEIN KINASE C; RHO KINASE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SPHINGOSINE 1 PHOSPHATE; SPHINGOSINE KINASE 1; SPHINGOSINE KINASE 2; UNCLASSIFIED DRUG; VASOPRESSIN V1A RECEPTOR;

ARACHIDONIC ACID METABOLISM; AUTOREGULATION; CALCIUM SIGNALING; CELLULAR DISTRIBUTION; CORONARY BLOOD VESSEL; DRUG MECHANISM; EVOKED MUSCLE RESPONSE; EXTRACELLULAR MATRIX; HEART DEPOLARIZATION; HEART FAILURE; HEART MUSCLE CONTRACTILITY; HUMAN; MECHANOTRANSDUCTION; MICROVASCULARIZATION; MOLECULAR DYNAMICS; MUSCLE DEVELOPMENT; MYOGENIC RESPONSE; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; REVIEW; SIGNAL TRANSDUCTION; TUNING CURVE; VASCULAR SMOOTH MUSCLE; VASOCONSTRICTION;

ANIMALS; BIODIVERSITY; CALCIUM SIGNALING; HUMANS; LYSOPHOSPHOLIPIDS; MUSCLE DEVELOPMENT; MUSCLE, SMOOTH, VASCULAR; PROTEIN KINASE C; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION; SPHINGOSINE;

EID: 84874236229     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvs345     Document Type: Review

References (116)

1. Yang J, Hossein Noyan-Ashraf M, Meissner A, Voigtlaender-Bolz J, Kroetsch JT, Foltz W et al. Proximal Cerebral arteries develop myogenic responsiveness in heart failure via tumor necrosis factor-alpha-dependent activation of sphingosine-1-phosphate signaling. Circulation 2012;126:196-206.
2. Meissner A, Yang J, Kroetsch JT, Sauve M, Dax H, Momen A et al. Tumor necrosis factor-a-mediated downregulation of the cystic fibrosis transmembrane conductance regulator drives pathological sphingosine-1-phosphate signaling in a mouse model of heart failure. Circulation 2012;125:2739-2750.
3. Hoefer J, Azam MA, Kroetsch JT, Poi HL, Momen MA, Voigtlaender-Bolz J et al. Sphingosine-1-phosphate-dependent activation of p38 MAPK maintains elevated peripheral resistance in heart failure through increased myogenic vasoconstriction. Circ Res 2010;107:923-933.
4. Bayliss WM. On the local reactions of the arterial wall to changes of internal pressure. J Physiol 1902;28:220-231.
5. Davis MJ, Hill MA. Signaling mechanisms underlying the vascular myogenic response. Physiol Rev 1999;79:387-423.
6. Schubert R, Mulvany MJ. The myogenic response: established facts and attractive hypotheses. Clin Sci (Lond) 1999;96:313-326.
7. Hill MA, Zou H, Potocnik SJ, Meininger GA, Davis MJ. Invited review: arteriolar smooth muscle mechanotransduction: Ca(2+) signaling pathways underlying myogenic reactivity. J Appl Physiol 2001;91:973-983.
8. Hill MA, Davis MJ, Meininger GA, Potocnik SJ, Murphy TV. Arteriolar myogenic signalling mechanisms: implications for local vascular function. Clin Hemorheol Microcirc 2006;34:67-79.
9. Schubert R, Lidington D, Bolz SS. The emerging role of Ca2+ sensitivity regulation in promoting myogenic vasoconstriction. Cardiovasc Res 2008;77:8-18.
10. Hill MA, Meininger GA, Davis MJ, Laher I. Therapeutic potential of pharmacologically targeting arteriolar myogenic tone. Trends Pharmacol Sci 2009;30:363-374.
11. Baek EB, Kim SJ. Mechanisms of myogenic response: Ca(2+)-dependent and-independent signaling. J Smooth Muscle Res 2011;47:55-65.
12. Cole WC,Welsh DG. Role of myosin light chain kinase and myosin light chain phosphatase in the resistance arterial myogenic response to intravascular pressure. Arch Biochem Biophys 2011;510:160-173.
13. Paulson OB, Strandgaard S, Edvinsson L. Cerebral autoregulation. Cerebrovasc Brain Metab Rev 1990;2:161-192.
14. Drummond JC. The lower limit of autoregulation: time to revise our thinking?. Anesthesiology 1997;86:1431-1433.
15. Bidani AK, Griffin KA, Williamson G, Wang X, Loutzenhiser R. Protective importance of the myogenic response in the renal circulation. Hypertension 2009;54: 393-398.
16. Moien-Afshari F, Skarsgard PL, McManus BM, Laher I. Cardiac transplantation and resistance artery myogenic tone. Can J Physiol Pharmacol 2004;82:840-848.
17. Metting PJ, Kostrzewski KA, Stein PM, Stoos BA, Britton SL. Quantitative contribution of systemic vascular autoregulation in acute hypertension in conscious dogs. J Clin Invest 1989;84:1900-1905.
18. Metting PJ, Stein PM, Stoos BA, Kostrzewski KA, Britton SL. Systemic vascular autoregulation amplifies pressor responses to vasoconstrictor agents. Am J Physiol 1989; 256:R98-R105.
19. Petersen HH, Choy J, Stauffer B, Moien-Afshari F, Aalkjaer C, Leinwand L et al. Coronary artery myogenic response in a genetic model of hypertrophic cardiomyopathy. Am J Physiol Heart Circ Physiol 2002;283:H2244-H2249.
20. Gschwend S, Henning RH, Pinto YM, de ZD, van Gilst WH, Buikema H. Myogenic constriction is increased in mesenteric resistance arteries from rats with chronic heart failure: instantaneous counteraction by acute AT1 receptor blockade. Br J Pharmacol 2003;139:1317-1325.
21. Ungvari Z, Pacher P, Kecskemeti V, Papp G, Szollar L, Koller A. Increased myogenic tone in skeletal muscle arterioles of diabetic rats. Possible role of increased activity of smooth muscle Ca2+ channels and protein kinase C. Cardiovasc Res 1999;43: 1018-1028.
22. Khavandi K, Greenstein AS, Sonoyama K, Withers S, Price A, Malik RA et al. Myogenic tone and small artery remodelling: insight into diabetic nephropathy. Nephrol Dial Transplant 2009;24:361-369.
23. Matrougui K, Schiavi P, Guez D, Henrion D. High sodium intake decreases pressure-induced (myogenic) tone and flow-induced dilation in resistance arteries from hypertensive rats. Hypertension 1998;32:176-179.
24. Hughes JM, Bund SJ. Arterial myogenic properties of the spontaneously hypertensive rat. Exp Physiol 2002;87:527-534.
25. Loutzenhiser RD, Parker MJ. Hypoxia inhibits myogenic reactivity of renal afferent arterioles by activating ATP-sensitive K+ channels. Circ Res 1994;74:861-869.
26. Wang H, Smeda JS, Lee RM. Prevention of stroke and preservation of the functions of cerebral arteries by treatment with perindopril in stroke-prone spontaneously hypertensive rats. Can J Physiol Pharmacol 1998;76:26-34.
27. Davis MJ, Donovitz JA, Hood JD. Stretch-activated single-channel and whole cell currents in vascular smooth muscle cells. Am J Physiol 1992;262:C1083-C1088.
28. Schubert R, Brayden JE. Stretch-activated Cation Channels and the Myogenic Response of Small Arteries. In: Kamkin A, Kiseleva I, eds. Mechanosensitivity in Cells and Tissues. Moscow: Academia, 2005.
29. Lucchesi PA, Sabri A, Belmadani S, Matrougui K. Involvement of metalloproteinases 2/9 in epidermal growth factor receptor transactivation in pressure-induced myogenic tone in mouse mesenteric resistance arteries. Circulation 2004;110:3587-3593.
30. Platts SH, Falcone JC, Holton WT, Hill MA, Meininger GA. Alteration of microtubule polymerization modulates arteriolar vasomotor tone. Am J Physiol 1999;277: H100-H106.
31. D'Angelo G, Mogford JE, Davis GE, Davis MJ, Meininger GA. Integrin-mediated reduction in vascular smooth muscle [Ca2+](i) induced by RGD-containing peptide. Am J Physiol 1997;272:H2065-H2070.
32. Mogford JE, Davis GE, Platts SH, Meininger GA. Vascular smooth muscle alpha(v)-beta(3) integrin mediates arteriolar vasodilation in response to RGD peptides. Circ Res 1996;79:821-826.
33. Mederos y Schnitzler M, Storch U, Meibers S, Nurwakagari P, Breit A, Essin K et al. Gq-coupled receptors as mechanosensors mediating myogenic vasoconstriction. EMBO J 2008;27:3092-3103.
34. Mederos y Schnitzler M, Storch U, Gudermann T. AT1 receptors as mechanosensors. Curr Opin Pharmacol 2011;11:112-116.
35. Jaggar JH, Wellman GC, Heppner TJ, Porter VA, Perez GJ, Gollasch M et al. Ca2+ channels, ryanodine receptors and Ca(2+)-activated K+ channels: a functional unit for regulating arterial tone. Acta Physiol Scand 1998;164:577-587.
36. Kauser K, Clark JE, Masters BS, Ortiz de Montellano PR, Ma YH, Harder DR et al. Inhibitors of cytochrome P-450 attenuate the myogenic response of dog renal arcuate arteries. Circ Res 1991;68:1154-1163.
37. Narayanan J, Imig M, Roman RJ, Harder DR. Pressurization of isolated renal arteries increases inositol trisphosphate and diacylglycerol. Am J Physiol 1994;266: H1840-H1845.
38. Jarajapu YP, Knot HJ. Role of phospholipase C in development of myogenic tone in rat posterior cerebral arteries. Am J Physiol Heart Circ Physiol 2002;283: H2234-H2238.
39. Zhang J, Wier WG, Blaustein MP. Mg2+ blocks myogenic tone but not K+-induced constriction: role for SOCs in small arteries. Am J Physiol Heart Circ Physiol 2002;283: H2692-H2705.
40. Dessy C, Matsuda N, Hulvershorn J, Sougnez CL, Sellke FW, Morgan KG. Evidence for involvement of the PKC-alpha isoform in myogenic contractions of the coronary microcirculation. Am J Physiol Heart Circ Physiol 2000;279:H916-H923.
41. Korzick DH, Laughlin MH, Bowles DK. Alterations in PKC signaling underlie enhanced myogenic tone in exercise-trained porcine coronary resistance arteries. J Appl Physiol 2004;96:1425-1432.
42. Schubert R, Kalentchuk VU, Krien U. Rho kinase inhibition partly weakens myogenic reactivity in rat small arteries by changing calcium sensitivity. Am J Physiol Heart Circ Physiol 2002;283:H2288-H2295.
43. Bolz SS, Vogel L, Sollinger D, Derwand R, Boer C, Pitson SM et al. Sphingosine kinase modulates microvascular tone and myogenic responses through activation of RhoA/Rho kinase. Circulation 2003;108:342-347.
44. Johnson RP, El-Yazbi AF, Takeya K, Walsh EJ, Walsh MP, Cole WC. Ca2+ sensitization via phosphorylation of myosin phosphatase targeting subunit at threonine-855 by Rho kinase contributes to the arterial myogenic response. J Physiol 2009;587: 2537-2553.
45. Davis MJ. Myogenic response gradient in an arteriolar network. Am J Physiol 1993; 264:H2168-H2179.
46. Golding EM, Robertson CS, Bryan RM. Comparison of the myogenic response in rat cerebral arteries of different calibers. Brain Res 1998;785:293-298.
47. Uchida E, Bohr DF. Myogenic tone in isolated perfused vessels. Occurrence among vascular beds and along vascular trees. Circ Res 1969;25:549-555.
48. Huang A, Sun D, Koller A, Kaley G. Gender difference in myogenic tone of rat arterioles is due to estrogen-induced, enhanced release of NO. Am J Physiol 1997;272: H1804-H1809.
49. Reimann K, Krishnamoorthy G, Wier WG, Wangemann P. Gender differences in myogenic regulation along the vascular tree of the gerbil cochlea. PLoS One 2011; 6:e25659.
50. Su BY, Reber KM, Nankervis CA, Nowicki PT. Development of the myogenic response in postnatal intestine: role of PKC. Am J Physiol Gastrointest Liver Physiol 2003;284:G445-G452.
51. Kang LS, Kim S, Dominguez JM, Sindler AL, Dick GM, Muller-Delp JM. Aging and muscle fiber type alter K+ channel contributions to the myogenic response in skeletal muscle arterioles. J Appl Physiol 2009;107:389-398.
52. Lott ME, Herr MD, Sinoway LI. Effects of age on brachial artery myogenic responses in humans. Am J Physiol Regul Integr Comp Physiol 2004;287:R586-R591.
53. Lagaud G, Gaudreault N, Moore ED, van Breemen C, Laher I. Pressure-dependent myogenic constriction of cerebral arteries occurs independently of voltagedependent activation. Am J Physiol Heart Circ Physiol 2002;283:H2187-H2195.
54. Lidington D, Peter BF, Meissner A, Kroetsch JT, Pitson SM, Pohl U et al. The phosphorylation motif at serine 225 governs the localization and function of sphingosine kinase 1 in resistance arteries. Arterioscler Thromb Vasc Biol 2009;29:1916-1922.
55. Mann DL. Sphingosine 1-phosphate as a therapeutic target in heart failure: more questions than answers. Circulation 2012;125:2692-2694.
56. Spiegel S, Milstien S. Sphingosine-1-phosphate: an enigmatic signalling lipid. Nat Rev Mol Cell Biol 2003;4:397-407.
57. Watterson K, Sankala H, Milstien S, Spiegel S. Pleiotropic actions of sphingosine-1-phosphate. Prog Lipid Res 2003;42:344-357.
58. Maceyka M, Harikumar KB, Milstien S, Spiegel S. Sphingosine-1-phosphate signaling and its role in disease. Trends Cell Biol 2012;22:50-60.
59. Mattie M, Brooker G, Spiegel S. Sphingosine-1-phosphate, a putative second messenger, mobilizes calcium from internal stores via an inositol trisphosphate-independent pathway. J Biol Chem 1994;269:3181-3188.
60. Hinkovska-Galcheva V, VanWay SM, Shanley TP, Kunkel RG. The role of sphingosine-1-phosphate and ceramide-1-phosphate in calcium homeostasis. Curr Opin Investig Drugs 2008;9:1192-1205.
61. Watterson KR, Ratz PH, Spiegel S. The role of sphingosine-1-phosphate in smooth muscle contraction. Cell Signal 2005;17:289-298.
62. Bolz SS, Pohl U. Highly effective non-viral gene transfer into vascular smooth muscle cells of cultured resistance arteries demonstrated by genetic inhibition of sphingosine-1-phosphate-induced vasoconstriction. J Vasc Res 2003;40:399-405.
63. Lorenz JN, Arend LJ, Robitz R, Paul RJ, MacLennan AJ. Vascular dysfunction in S1P2 sphingosine 1-phosphate receptor knockout mice. Am J Physiol Regul Integr Comp Physiol 2007;292:R440-R446.
64. Coussin F, Scott RH, Wise A, Nixon GF. Comparison of sphingosine 1-phosphate-induced intracellular signaling pathways in vascular smooth muscles: differential role in vasoconstriction. Circ Res 2002;91:151-157.
65. Skoura A, Hla T. Regulation of vascular physiology and pathology by the S1P2 receptor subtype. Cardiovasc Res 2009;82:221-228.
66. van der Giet M, Tolle M, Kleuser B. Relevance and potential of sphingosine-1-phosphate in vascular inflammatory disease. Biol Chem 2008;389:1381-1390.
67. Hla T, Brinkmann V. Sphingosine 1-phosphate (S1P): Physiology and the effects of S1P receptor modulation. Neurology 2011;76:S3-S8.
68. Xia P, Wang L, Moretti PA, Albanese N, Chai F, Pitson SM et al. Sphingosine kinase interacts with TRAF2 and dissects tumor necrosis factor-alpha signaling. J Biol Chem 2002;277:7996-8003.
69. Pitson SM, Xia P, Leclercq TM, Moretti PA, Zebol JR, Lynn HE et al. Phosphorylation-dependent translocation of sphingosine kinase to the plasma membrane drives its oncogenic signalling. J Exp Med 2005;201:49-54.
70. Stahelin RV, Hwang JH, Kim JH, Park ZY, Johnson KR, Obeid LM et al. The mechanism of membrane targeting of human sphingosine kinase 1. J Biol Chem 2005;280: 43030-43038.
71. Sutherland CM, Moretti PA, Hewitt NM, Bagley CJ, Vadas MA, Pitson SM. The calmodulin-binding site of sphingosine kinase and its role in agonist-dependent translocation of sphingosine kinase 1 to the plasma membrane. J Biol Chem 2006;281: 11693-11701.
72. Kusner DJ, Thompson CR, Melrose NA, Pitson SM, Obeid LM, Iyer SS. The localization and activity of sphingosine kinase 1 are coordinately regulated with actin cytoskeletal dynamics in macrophages. J Biol Chem 2007;282:23147-23162.
73. Hengst JA, Guilford JM, Fox TE, Wang X, Conroy EJ, Yun JK. Sphingosine kinase 1 localized to the plasma membrane lipid raft microdomain overcomes serum deprivation induced growth inhibition. Arch Biochem Biophys 2009;492:62-73.
74. Ter Braak M, Danneberg K, Lichte K, Liphardt K, Ktistakis NT, Pitson SM et al. Galpha(q)-mediated plasma membrane translocation of sphingosine kinase-1 and cross-activation of S1P receptors. Biochim Biophys Acta 2009;1791:357-370.
75. Jarman KE, Moretti PA, Zebol JR, Pitson SM. Translocation of sphingosine kinase 1 to the plasma membrane is mediated by calcium-and integrin-binding protein 1. J Biol Chem 2010;285:483-492.
76. Pitson SM. Regulation of sphingosine kinase and sphingolipid signaling. Trends Biochem Sci 2011;36:97-107.
77. Safadi-Chamberlain F, Wang LP, Payne SG, Lim CU, Stratford S, Chavez JA et al. Effect of a membrane-targeted sphingosine kinase 1 on cell proliferation and survival. Biochem J 2005;388:827-834.
78. Xin C, Ren S, Pfeilschifter J, Huwiler A. Heterologous desensitization of the sphingosine-1-phosphate receptors by purinoceptor activation in renal mesangial cells. Br J Pharmacol 2004;143:581-589.
79. Casabona G. Intracellular signal modulation: a pivotal role for protein kinase C. Prog Neuropsychopharmacol Biol Psychiatry 1997;21:407-425.
80. Salamanca DA, Khalil RA. Protein kinase C isoforms as specific targets for modulation of vascular smooth muscle function in hypertension. Biochem Pharmacol 2005; 70:1537-1547.
81. Earley S, Straub SV, Brayden JE. Protein kinase C regulates vascular myogenic tone through activation of TRPM4. Am J Physiol Heart Circ Physiol 2007;292: H2613-H2622.
82. Crozatier B. Central role of PKCs in vascular smooth muscle cell ion channel regulation. J Mol Cell Cardiol 2006;41:952-955.
83. Karibe A, Watanabe J, Horiguchi S, Takeuchi M, Suzuki S, Funakoshi M et al. Role of cytosolic Ca2+ and protein kinase C in developing myogenic contraction in isolated rat small arteries. Am J Physiol 1997;272:H1165-H1172.
84. Wesselman JP, Spaan JA, Van Der Meulen ET, VanBavel E. Role of protein kinase C in myogenic calcium-contraction coupling of rat cannulated mesenteric small arteries. Clin Exp Pharmacol Physiol 2001;28:848-855.
85. Chang K, Xiao D, Huang X, Longo LD, Zhang L. Chronic hypoxia increases pressure-dependent myogenic tone of the uterine artery in pregnant sheep: role of ERK/PKC pathway. Am J Physiol Heart Circ Physiol 2009;296:H1840-H1849.
86. Baek EB, Jin C, Park SJ, Park KS, Yoo HY, Jeon JH et al. Differential recruitment of mechanisms for myogenic responses according to luminal pressure and arterial types. Pflugers Arch 2010;460:19-29.
87. Maasch C, Wagner S, Lindschau C, Alexander G, Buchner K, Gollasch M et al. Protein kinase calpha targeting is regulated by temporal and spatial changes in intracellular free calcium concentration [Ca(2+)](i). FASEB J 2000;14:1653-1663.
88. Kashihara T, Nakayama K, Ishikawa T. Distinct roles of protein kinase C isoforms in myogenic constriction of rat posterior cerebral arteries. J Pharmacol Sci 2008;108: 446-454.
89. Zou Y, Akazawa H, Qin Y, Sano M, Takano H, Minamino T et al. Mechanical stress activates angiotensin II type 1 receptor without the involvement of angiotensin II. Nat Cell Biol 2004;6:499-506.
90. Rakesh K, Yoo B, Kim IM, Salazar N, Kim KS, Rockman HA. beta-Arrestin-biased agonism of the angiotensin receptor induced by mechanical stress. Sci Signal 2010; 3:ra46.
91. Yasuda N, Miura S, Akazawa H, Tanaka T, Qin Y, Kiya Y et al. Conformational switch of angiotensin II type 1 receptor underlying mechanical stress-induced activation. EMBO Rep 2008;9:179-186.
92. Zhang YL, Frangos JA, Chachisvilis M. Mechanical stimulus alters conformation of type 1 parathyroid hormone receptor in bone cells. Am J Physiol Cell Physiol 2009; 296:C1391-C1399.
93. Makino A, Prossnitz ER, Bunemann M, Wang JM, Yao W, Schmid-Schonbein GW. G protein-coupled receptors serve as mechanosensors for fluid shear stress in neutrophils. Am J Physiol Cell Physiol 2006;290:C1633-C1639.
94. Abdul-Majeed S, Nauli SM. Dopamine receptor type 5 in the primary cilia has dual chemo-and mechano-sensory roles. Hypertension 2011;58:325-331.
95. Nowycky MC, Thomas AP. Intracellular calcium signaling. J Cell Sci 2002;115: 3715-3716.
96. Croxton TL, Lande B, Hirshman CA. Role of G proteins in agonist-induced Ca2+ sensitization of tracheal smooth muscle. Am J Physiol 1998;275:L748-L755.
97. Momotani K, Artamonov MV, Utepbergenov D, Derewenda U, Derewenda ZS, Somlyo AV. p63RhoGEF couples G{alpha}q/11-mediated signaling to ca2+ sensitization of vascular smooth muscle contractility. Circ Res 2011;109:993-1002.
98. Anfinogenova Y, Brett SE,Walsh MP, Harraz OF,Welsh DG. Do TRPC-like currents and G protein-coupled receptors interact to facilitate myogenic tone development? Am J Physiol Heart Circ Physiol 2011;301:H1378-H1388.
99. Orr AW, Hastings NE, Blackman BR,Wamhoff BR. Complex regulation and function of the inflammatory smooth muscle cell phenotype in atherosclerosis. J Vasc Res 2010;47:168-180.
100. Savoia C, Burger D, Nishigaki N, Montezano A, Touyz RM. Angiotensin II and the vascular phenotype in hypertension. Expert Rev Mol Med 2011;13:e11.
101. Alexander MR, Owens GK. Epigenetic control of smooth muscle cell differentiation and phenotypic switching in vascular development and disease. Annu Rev Physiol 2012;74:13-40.
102. McDonald OG, Owens GK. Programming smooth muscle plasticity with chromatin dynamics. Circ Res 2007;100:1428-1441.
103. Kang H, Hata A. MicroRNA regulation of smooth muscle gene expression and phenotype. Curr Opin Hematol 2012;19:224-231.
104. Xie C, Zhang J, Chen YE. MicroRNA and vascular smooth muscle cells. Vitam Horm 2011;87:321-339.
105. Halka AT, Turner NJ, Carter A, Ghosh J, Murphy MO, Kirton JP et al. The effects of stretch on vascular smooth muscle cell phenotype in vitro. Cardiovascular Pathology 2008;17:98-102.
106. Martinez-Lemus LA, Hill MA, Bolz SS, Pohl U, Meininger GA. Acute mechanoadaptation of vascular smooth muscle cells in response to continuous arteriolar vasoconstriction: implications for functional remodeling. FASEB J 2004;18:708-710.
107. Martinez-Lemus LA. The dynamic structure of arterioles. Basic Clin Pharmacol Toxicol 2012;110:5-11.
108. Pan S. Molecular mechanisms responsible for the atheroprotective effects of laminar shear stress. Antioxid Redox Signal 2009;11:1669-1682.
109. Lincoln TM, Wu X, Sellak H, Dey N, Choi CS. Regulation of vascular smooth muscle cell phenotype by cyclic GMP and cyclic GMP-dependent protein kinase. Front Biosci 2006;11:356-367.
110. Kingwell B, Boutouyrie P. Genetic influences on the arterial wall. Clin Exp Pharmacol Physiol 2007;34:652-657.
111. Yasmin, O'Shaughnessy KM. Genetics of arterial structure and function: towards new biomarkers for aortic stiffness? Clin Sci (Lond) 2008;114:661-677.
112. Majesky MW. Developmental basis of vascular smooth muscle diversity. Arterioscler Thromb Vasc Biol 2007;27:1248-1258.
113. Zhang H, Gu S, Al-Sabeq B, Wang S, He J, Tam A et al. Origin-specific epigenetic program correlates with vascular bed-specific differences in Rgs5 expression. FASEB J 2012;26:181-191.
114. van Oostrom O, Fledderus JO, de KD, Pasterkamp G, Verhaar MC. Smooth muscle progenitor cells: friend or foe in vascular disease? Curr Stem Cell Res Ther 2009;4: 131-140.
115. Kacem K, Sercombe R. Differing influence of sympathectomy on smooth muscle cells and fibroblasts in cerebral and peripheral muscular arteries. Auton Neurosci 2006;124:38-48.
116. Jiao L, Wang MC, Yang YA, Chen EQ, Xu HT, Wu KY et al. Norepinephrine reversibly regulates the proliferation and phenotypic transformation of vascular smooth muscle cells. Exp Mol Pathol 2008;85:196-200.